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The Influence of Diet and Environment on the Gut Microbial Community of Field Crickets

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The Influence of Diet and Environment on the Gut Microbial Community of Field Crickets Received: 8 January 2018 | Revised: 7 February 2018 | Accepted: 9 February 2018 DOI: 10.1002/ece3.3977 ORIGINAL RESEARCH The influence of diet and environment on the gut microbial community of field crickets Soon Hwee Ng1 | Michael Stat2,3 | Michael Bunce3 | Leigh W. Simmons1 1Centre for Evolutionary Biology, School of Biological Sciences, University of Western Abstract Australia, Crawley, Australia The extent to which diet and environment influence gut community membership 2 Department of Biological (presence or absence of taxa) and structure (individual taxon abundance) is the sub- Sciences, Macquarie University, Sydney, Australia ject of growing interest in microbiome research. Here, we examined the gut bacterial 3Trace and Environmental DNA (TrEnD) communities of three cricket groups: (1) wild caught field crickets, (2) laboratory- Laboratory, Department of Environment reared crickets fed cat chow, and (3) laboratory- reared crickets fed chemically de- and Agriculture, Curtin University, Perth, Australia fined diets. We found that both environment and diet greatly altered the structure of the gut bacterial community. Wild crickets had greater gut microbial diversity and Correspondence Soon Hwee Ng, Centre for Evolutionary higher Firmicutes to Bacteroidetes ratios, in contrast to laboratory- reared crickets. Biology, School of Biological Sciences, Predictive metagenomes revealed that laboratory- reared crickets were significantly University of Western Australia, Crawley, Australia. enriched in amino acid degradation pathways, while wild crickets had a higher rela- Email: [email protected] tive abundance of peptidases that would aid in amino acid release. Although wild and laboratory animals differ greatly in their bacterial communities, we show that the community proportional membership remains stable from Phylum to Family taxo- nomic levels regardless of differences in environment and diet, suggesting that en- dogenous factors, such as host genetics, have greater control in shaping gut community membership. KEYWORDS community membership, community structure, diet, gut microbial diversity, predictive metagenomes, Teleogryllus oceanicus 1 | INTRODUCTION & Brune, 2012; Vargas- Asensio et al., 2014). The ability of gut mi- crobes to supplement the host genome with functional genes is be- Metazoans live symbiotically with microorganisms on and within lieved to promote the exploitation of food previously unavailable to them (Hacquard et al., 2015), and the gastrointestinal tract is one of the host, leading to ecological isolation and divergence from those the most studied organs for these symbiotic interactions (Douglas, species that lack microbial symbionts (Brucker & Bordenstein, 2012; 2015; Engel & Moran, 2013; Leslie & Young, 2015). Gut microbes Janson, Stireman, Singer, & Abbot, 2008). are known to be vital for species feeding on specialized or subop- Shifts in gut microbial communities occur in two major ways: timal diets by providing essential nutrition (amino acids, vitamins) change in community membership (presence or absence of micro- (Douglas, 2006, 2009; Wigglesworth, 1936), or aiding in degra- bial taxa) and change in community structure (relative abundance of dation of otherwise indigestible plant cell walls (Douglas, 2009; microbial taxa); two communities can have the same memberships Genta, Dillon, Terra, & Ferreira, 2006; Kohler, Dietrich, Scheffrahn, but different structures, but if memberships of communities are This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 4704 | www.ecolevol.org Ecology and Evolution. 2018;8:4704–4720. NG ET AL. | 4705 different, they will have different structures (Schloss & Handelsman, Bacteroidetes) to increase (Daniel et al., 2014). Moreover, the diver- 2006). A related idea is the proportional membership, which is de- sity of the microbial population in the habitat could influence the rived from a study by Zhao, Irwin, and Dong (2016); the authors types of microbes that colonize the gut. For instance, animals housed counted the taxa detected and summarized the types of taxa that in laboratory conditions have a less diverse gut microbial community constitute the gut community membership as proportions at phylum and a reduced subset of that found in their wild counterparts (Belda level. For example, in a gut where there are 100 different bacterial et al., 2011; Chandler et al., 2011; Lehman, Lundgren, & Petzke, species, a proportional membership of 50% for Firmicutes implies 2009; Pérez- Cobas et al., 2015; Staubach, Baines, Kunzel, Bik, & that 50 species are identified to that phylum. It was also demon- Petrov, 2013; Xiang et al., 2006). Yet, despite much variability in gut strated that proportional membership was consistent among differ- microbial profiles, there appears to be a core microbiome in many ent individuals in a population and showed less fluctuation than the species (Berg et al., 2016; Pérez- Cobas et al., 2015; Roeselers et al., community structure within an individual in a longitudinal survey 2011; Shade & Handelsman, 2012; Tinker & Ottesen, 2016; Wang (Zhao et al., 2016). Figure 1 uses a hypothetical example to illus- et al., 2016), that is hypothesized to be the result of co- evolution of trate the different descriptors of microbial communities based on beneficial gut microbes with their hosts (Shapira, 2016). sequencing data analysis and used throughout this study. The effect of diet on life history traits has been well documented, Pronounced interpopulation and interindividual variations in the especially in the trade- offs between trait expressions due to differ- gut microbial communities are observed in many species, with con- ential allocation of limiting internal nutrients (Boggs & Ross, 1993; tributions from endogenous factors, such as age, sex and genotype, Cotter, Simpson, Raubenheimer, & Wilson, 2011; Kupferberg, Marks, and exogenous factors, including habitat and diet (Bennett et al., & Power, 1994; Zera & Harshman, 2001). In recent years, crickets 2016; Han, Lee, Jeong, Jeon, & Hyun, 2017; Kovacs et al., 2011). As are emerging as a useful model organism for studying sexually se- gut microbes can help in the digestion of ingested food, changes in lected traits and elucidating the effects of diet quality and com- gut microbial populations could entail a shift in the genes that carry position on trade- offs between life history traits and sexual traits out metabolic reactions in the gastrointestinal tract, which could im- (Gray & Eckhardt, 2001; Harrison, Raubenheimer, Simpson, Godin, pact the food utilization efficiency of the host (Holm et al., 2016; & Bertram, 2014; Kelly, Neyer, & Gress, 2014; Lyn, Naikkhwah, Turnbaugh et al., 2006). Aksenov, & Rollo, 2011; Maklakov et al., 2008; Simmons, 2011). But Host genetics are believed to influence the gut microbial com- few studies have examined the impact of the gut microbiome on fit- munity, as gut microbiota has been shown to be more similar among ness in crickets. The first report on gut microbiota of crickets dates family members and even within populations (Turnbaugh et al., back to 1981 (Ulrich, Buthala, & Klug, 1981), and subsequent studies 2009; Zhao et al., 2016). But early twin studies have produced in- between 1989 and 1998 have revealed broad categories of bacterial consistent results. For example, Stewart, Chadwick, and Murray communities in the gut, and general changes in its composition in (2005) observed a higher degree of similarity in the gut microbiota response to changes in diet (Kaufman & Klug, 1991; Kaufman, Klug, of monozygotic twins compared with dizygotic twins and unrelated & Merritt, 1989; Santo Domingo, 1998; Santo Domingo, Kaufman, pairs. Yet, it has been reported that the gut microbiota of monozy- Klug, & Tiedje, 1998; Santo Domingo, Kaufman, Klug, Holben, et al., gotic twins is no more similar than the microbiota of dizygotic twins 1998). In addition, Kaufman and Klug (1991) found that the pres- (Turnbaugh et al., 2009; Yatsunenko et al., 2012). Nevertheless, ence of gut bacteria increased the digestive efficiency of plant poly- recent studies, through reanalysis of previous data (Goodrich saccharides and allowed crickets to utilize a wider range of dietary et al., 2014; Zhao et al., 2016) and genomewide association studies carbohydrates. Only very recently, however, with the prevalence of (Davenport, 2016; Davenport et al., 2015), provide compelling evi- next- generation sequencing, have detailed examinations of gut mi- dence that host genetics is a factor that shapes the gut microbiota. crobiota been possible (Smith, Srygley, Dietrich, & Mueller, 2016; Moreover, Zhao et al. (2016) demonstrated that host genetics are Smith, Srygley, Healy, Swaminath, & Mueller, 2017). In Mormon fundamentally responsible for gut community membership, leaving crickets and decorated crickets, mating, but not protein consump- nongenetic factors to regulate the abundance of different microbes. tion, was found to influence gut microbial structure (Smith et al., Host diet is a major exogenous factor in shifting the structure of 2016). the gut bacterial community and its metabolic capabilities (Bolnick, To understand how exogenous and endogenous factors influ- Snowberg, Hirsch, Lauber, Knight, et al., 2014; Chandler, Lang, ence gut bacterial communities in
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